Mechanisms of repair of polycyclic aromatic hydrocarbon-induced DNA damage

The Carcinogenic Effects of Polycyclic Aromatic Hydrocarbons

Volumn , Issue , 2005, Pages 211-258

  Naegeli, Hanspeter ^a   Geacintov, Nicholas E ^b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84967644790     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1142/9781860949333_0006     Document Type: Chapter

References (130)

1. Conney AH (1982) Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons. Cancer Res. 42: 4875-4917.
2. Phillips DH and Grover PL (1994) Polycyclic aromatic hydrocarbon activation: bay regions and beyond. Drug Metab. Rev. 26: 443-467.
3. Sims P, Grover PL, Swaisland A, Pal K and Hewer A (1974) Metabolic activation of benzo[a]pyrene proceeds by a diol-epoxide. Nature 252: 326-328.
4. Peltonen K and Dipple A (1995) Polycyclic aromatic hydrocarbons: chemistry of DNA adduct formation. J. Occup. Environ. Med. 37: 52-58.
5. Szeliga J and Dipple A (1998) DNA adduct formation by polycyclic aromatic hydrocarbon dihydrodiol epoxides. Chem. Res. Toxicol. 11: 1-11.
6. De Boer J, Andressoo JO, de Wit J, Huijmans J, Beems RB, van Steeg H, Weeda G, van der Horst GTJ, van Leeuwen W, Themmen APN, Meradji M and Hoeijmakers JHJ (2002) Premature aging in mice deficient in DNA repair and transcription. Science 296: 1276-1279.
7. Bigger CA, Flickinger DJ, St John J, Harvey RG and Dipple A (1991) Preferential mutagenesis at G.C base pairs by the anti 3,4-dihydrodiol 1,2-epoxide of 7-methylbenz[a]anthracene. Mol. Carcinog. 4: 176-179.
8. Glatt H, Harvey RG, Phillips DH, Hewer A and Grover PL (1989) Influence of the alkyl substituent on mutagenicity and covalent DNA binding of bay region diolepoxides of 7-methyl- and 7-ethylbenz[a]anthracene in Salmonella and V79 Chinese hamster cells. Cancer Res. 49: 1778-1782.
9. Yan S, Shapiro R, Geacintov NE and Broyde S (2001) Stereochemical, structural, and thermodynamic origins of stability differences between stereoisomeric benzo[a]pyrene diol epoxide deoxyadenosine adducts in a DNA mutational hot spot sequence. J. Am. Chem. Soc. 123: 7054-7066.
10. Vogelstein B and Kinzler KW (1993) The multistep nature of cancer. Trends Genet. 9: 138-141.
11. Drinkwater NR, Miller EC and Miller JA (1980) Estimation of apurinic/apyrimidinic sites and phosphotriesters in deoxyribonucleic acid treated with electrophilic carcinogens and mutagens. Biochemistry 19: 5087-5092.
12. Lawley PD and Brookes P (1963) Further studies on the alkylation of nucleic acids and their constituent nucleotides. Biochem J. 89: 127-138.
13. Chakravarti D, Pelling JC, Cavalieri EL and Rogan EG (1995) Relating aromatic hydrocarbon-induced DNA adducts and c-H-ras mutations in mouse skin papillomas: the role of apurinic sites. Proc. Natl. Acad. Sci. USA 92: 10422-10426.
14. Braithwaite E, Wu X and Wang Z (1998) Repair of DNA lesions induced by polycyclic aromatic hydrocarbons in human cell-free extracts: involvement of two excision repair mechanisms in vitro. Carcinogenesis 19: 1239-1246.
15. Melendez-Colon VJ, Luch A, Seidel A and Baird WM (1999) Cancer initiation by polycyclic aromatic hydrocarbons results from formation of stable DNA adducts rather than apurinic sites. Carcinogenesis 20: 1885-1891.
16. Sancar A (1996) DNA excision repair. Annu. Rev. Biochem. 65: 43-81.
17. Wood RD (1997) Nucleotide excision repair in mammalian cells. J. Biol. Chem. 272: 23465-23468.
18. Huang JC, Svoboda D, Reardon JT and Sancar (1992) Human nucleotide excision nuclease removes thymine dimers from DNA by incising the 22nd phosphodiester bond 5′ and the 6th phosphodiester bond 3′ to the photodimer. Proc. Natl. Acad. Sci. USA 89: 3664-3668.
19. De Boer J and Hoeijmakers JH (2000) Nucleotide excision repair and human syndromes. Carcinogenesis 21: 453-460.
20. Friedberg EC (2001) How nucleotide excision repair protects against cancer. Nat. Rev. Cancer 1: 22-33.
21. Lin JJ and Sancar A (1992) (A)BC excinuclease: the Escherichia coli nucleotide excision repair enzyme. Mol. Microbiol. 6: 2219-2224.
22. Araujo SJ, Tirode F, Coin F, Pospiech H, Syväoja JE, Stucki M, Hübscher U, Egly JM and Wood RD (2000) Nucleotide excision repair of DNA with recombinant human proteins: definition of the minimal set of factors, active forms of TFIIH, and modulation by CAK. Genes Dev. 14: 349-359.
23. Mu D, Park CH, Matsunaga T, Hsu DS, Reardon JT and Sancar A (1995) Reconstitution of human DNA repair excision nuclease in a highly defined system. J. Biol. Chem. 270: 2415-2418.
24. Batty D, Rapic’-Otrin V, Levine AS and Wood RD (2000) Stable binding of human XPC complex to irradiated DNA confers strong discrimination for damaged sites. J. Mol. Biol. 300: 275-290.
25. Sugasawa K, Ng JM, Masutani C, Iwai S, van der Spek PJ, Eker AP, Hanaoka F, Bootsma D and Hoeijmakers JH (1998) Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol. Cell 2: 223-232.
26. Volker M, Moné MJ, Karmakar P, van Hoffen A, Schul W, Vermeulen W, Hoeijmakers JH, van Driel R, van Zeeland AA and Mullenders LH (2001) Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell 8: 213-224.
27. Yokoi M, Masutani C, Maekawa T, Sugasawa K, OhkumaY and Hanaoka F (2000) The xeroderma pigmentosum group C protein complex XPC-HR23B plays an important role in the recruitment of transcription factor IIH to damaged DNA. J. Biol. Chem. 275: 9870-9875.
28. Tang JY, Hwang BJ, Ford JM, Hanawalt PC and Chu J (2000) Xeroderma pigmentosum p48 gene enhances genomic repair and suppresses UV-induced mutagenesis. Mol. Cell 5:737-744.
29. Missura M, Buterin T, Hindges R, Hübscher U, Kaspárková J, Brabec V and Naegeli H (2001) Double-check probing of DNA bending and unwinding by XPA-RPA: an architectural function in DNA repair. EMBO J. 20:3554-3564.
30. De Laat WL, Appeldoom E, Sugasawa K, Weterings E, Jaspers NG and Hoeijmakers JH (1998) DNA binding polarity of human replication protein A positions nucleases in nucleotide excision repair. Genes Dev. 12: 2598-2609.
31. Reardon JT and Sancar A (2002) Molecular anatomy of the human excision nuclease assembled at sites of DNA damage. Mol. Cell. Biol. 22: 5938-5945.
32. Schultz P, Fribourg S, Poterszman A, Mallouh V, Moras D and Egly JM (2000) Molecular structure of human TFIIH. Cell 102: 599-607.
33. Evans E, Moggs JG, Hwang JR, Egly JM and Wood RD (1997) Mechanism of open complex and dual incision formation by human nucleotide excision repair factors. EMBO J. 16: 6559-6573.
34. Mu D, Wakasugi M, Hsu DS and Sancar A (1997) Characterization of reaction intermediates of human excision repair nuclease. J. Biol. Chem. 272: 121971-121979.
35. Jawhari A, Laine JP, Dubaele S, Lamour V, Poterszman A, Coin F, Moras D and Egly JM (2002) P52 mediates XPB function within the transcription/repair factor TFHH. J. Biol. Chem. 277: 31761-31767.
36. You JS, Wang M and Lee SH (2003) Biochemical analysis of the damage recognition process in nucleotide excision repair. J. Biol. Chem. 278: 7476-7485.
37. Drapkin R and Reinberg D (1994) The multifunctional TFIIH complex and transcriptional control. Trends Biochem. Sci. 19: 504-508.
38. Shivji MK, Podust VN, Hübscher U and Wood RD (1995) Nucleotide excision repair DNA synthesis by DNA polymerase epsilon in the presence of PCNA, RFC, and RPA. Biochemistry 34: 5011-5017.
39. Bohr VA, Smith CA, Okumoto DS and Hanawalt PC (1985) DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40: 359-369.
40. Ford JM, Lommel L and Hanawalt PC (1994) Preferential repair of ultraviolet light-induced DNA damage in the transcribed strand of the human p53 gene. Mol. Carcinog. 10: 105-109.
41. Tomaletti S and Pfeifer GP (1994) Slow repair of pyrimidine dimers at p53 mutation hotspots in skin cancer. Science 263: 1436-1438.
42. Mellon I, Spivak G and Hanawalt PC (1987) Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 51: 241-249.
43. Chen RH, Maher VM and McCormick JJ (1990) Effect of excision repair by diploid human fibroblasts on the kinds and locations of mutations induced by (±)-7β,8α-dihydroxy-9α, 10α-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene in the coding region of the HPRT gene. Proc. Natl. Acad. Sci. USA 87: 8680-8684.
44. Denissenko MF, Pao A, Pfeifer GP and Tang MS (1998) Slow repair of bulky DNA adducts along the nontranscribed strand of the human p53 gene may explain the strand bias of transversion mutations in cancers. Oncogene 16: 1241-1247.
45. Tang MS, Pao A and Zhang XS (1994) Repair of benzo[a]pyrene diol epoxide- and UV-induced DNA damage in dihydrofolate reductase and adenine phosphoribosyltransferase genes of CHO cells. J. Biol. Chem. 269: 12749-12754.
46. Carothers AM, Zhen W, Mucha J, Zhang YJ, Santella RM, Grunberger D and Bohr VA (1992) DNA strand-specific repair of (±)-3α,4β-dihydroxy-1α,20- epoxy-1,2,3,4-tetrahydrobenzo[c]phenanthrene adducts in the hamster dihydrofolate reductase gene. Proc. Natl. Acad. Sci. USA 89: 11925-11929.
47. Venema J, van Hoffen A, Karcagi V, Natarajan AT, van Zeeland AA and Mullenders LH (1991) Xeroderma pigmentosum complementation group C cells remove pyrimidine dimers selectively from the transcribed strand of active genes. Mol. Cell. Biol. 11: 4128-4134.
48. Gowen LC, Avrutskaya AV, Latour AM, Koller BH and Leadon SA (1998) BRCA1 required for transcription-coupled repair of oxidative DNA damage. Science 281: 1009-1012. (retracted).
49. Le Page F, Kwoh EE, Avrutskaya A, Gentil A, Leadon SA, Sarasin A and Cooper PK (2000) Transcription-coupled repair of 8-oxoguanine: requirement for XPG, TFIIH, and CSB and implications for Cockayne syndrome. Cell 101: 159-171.
50. Mellon I, Fajpal DK and Koi M (1996) Transcription-coupled repair deficiency and mutations in human mismatch repair genes. Science 272: 557-560.
51. Hasty P, Campisi J, Hoeijmakers JH, van Steeg H and Vijg J (2002) Aging and genome maintenance: lessons from the mouse? Science 299: 1355-1359.
52. 6 at the second position of N-ras codon 61. J. Biol. Chem. 10: 4990-5000.
53. Moriya M, Spiegel S, Fernandes A, Amin S, Liu T, Geacintov NE and Grollman AP (1996) Fidelity of translesional synthesis past benzo[a]pyrene diol epoxide-2′-deoxyguanosine DNA adducts: marked effects of host cell, sequence context, and chirality. Biochemistry 35: 16646-16651.
54. Seo KY, Jelinsky SA and Loechler EL (2000) Factors that influence the mutagenic patterns of DNA adducts from chemical carcinogens. Mutat. Res. 463: 215-246.
55. Wei SJ, Chang RL, Hennig E, Cui XX, Merkler KA, Wong CQ, Yagi H, Jerina DM and Conney AH (1994) Mutagenic selectivity at the HPRT locus in V-79 cells: comparison of mutations caused by bay-region benzo[a]pyrene 7,8- diol-9,10-epoxide enantiomers with high and low carcinogenic activity. Carcinogenesis 15: 1729-1735.
56. Wei D, Maher VM and McCormick JJ (1995) Site-specific rates of excision repair of benzo[a]pyrene diol epoxide adducts in the hypoxanthine phos- phoribosyltransferase gene of human fibroblasts: correlation with mutation spectra. Proc. Natl. Acad. Sci. USA 92: 2204-2208.
57. Friedberg EC, Walker GC and Siede W (1995) DNA Repair and Mutagenesis. ASM Press, Washington D.C.
58. Kraemer KH, Lee MM, Andrews AD and Lambert WC (1994) The role of sunlight and DNA repair in melanoma and nonmelanoma skin cancer. Arch. Dermatol. 130: 1018-1021.
59. De Vries A, van Oostrom CT, Hofhuis FM, Dortant PM, Berg RJ, de Gruijl FR, Wester PW, van Kreijl CF, Capel PJ, van Steeg H and Verbeek SJ (1995) Increased susceptibility to ultraviolet-B and carcinogens of mice lacking the DNA excision repair gene XPA. Nature 377: 169-173.
60. DeVries A, van Oostrom CT, Dortant PM, Beems RB, van Kreijl CF, Capel PJ and van Steeg H (1997) Spontaneous liver tumors and benzo[a]pyrene- induced lymphomas in XPA-deficient mice. Mol. Carcinog. 19: 46-53.
61. Nakane H, Takeuchi S, Yuba S, Saijo M, Nakatsu Y, Murai H, Nakatsuru Y, Ishikawa T, Hirota S, Kitamura Y, Kato Y, Tsunodo Y, Miyauchi H, Horio T, Tokunaja T, Matsunaga T, Nikaido O, Nishimune Y, Okada Y and Tanaka K (1994) High incidence of ultraviolet-B- or chemical-carcinogen-induced skin tumors in mice lacking the xeroderma pigmentosum group A gene. Nature 377: 165-168.
62. Adimoolam S and Ford JM (2002) P53 and DNA damage-inducible expression of the xeroderma pigmentosum group C gene. Proc. Natl. Acad. Sci. USA 99: 12985-12990.
63. Lloyd DR and Hanawalt PC (2002) P53 controls global nucleotide excision repair of low levels of structurally diverse benzo[g]chrysene-DNA adducts in human fibroblasts. Cancer Res. 62: 5288-5294.
64. Ford JM and Hanawalt PC (1995) Li-Fraumeni syndrome fibroblasts homozygous for p53 mutations are deficient in global DNA repair but exhibit normal transcription-coupled repair and enhanced UV resistance. Proc. Natl. Acad. Sci. USA 92: 8876-8880.
65. Ford JM and Hanawalt PC (1999) Expression of p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc. Natl. Acad. Sci. USA 96: 424-428.
66. Hess MT, Schwitter U, Petretta M, Giese B and Naegeli H (1996) Site-specific DNA substrates for human excision repair: comparison between deoxyribose and base adducts. Chem. Biol. 3: 121-128.
67. 2-dG adduct stereoisomers located within the human K-ras codon 12 sequence. Biochemistry 38: 569-581.
68. Buterin T, Hess MT, Luneva N, Geacintov NE, Amin S, Kroth H, Seidel A and Naegeli H (2000) Unrepaired fjord region polycyclic aromatic hydrocarbon- DNA adducts in ras codon 61 mutational hot spots. Cancer Res. 60: 1849-1856.
69. Hess MT, Gunz D, Luneva N, Geacintov NE and Naegeli H (1997) Base pair conformation-dependent excision of benzo[a]pyrene diol epoxide-guanine adducts by human nucleotide excision repair enzymes. Mol. Cell. Biol. 17: 7069-7076.
70. Thakker DR, Yagi H, Akagi H, Koreeda M, Lu AY, Levin W, Wood AW, Conney AH and Jerina DM (1977) Metabolism of benzo[a]pyrene. VI. Stereoselective metabolism of benzo[a]pyrene and benzo[a]pyrene 7,8- dihydrodiol to diol epoxides. Chem.-Biol. Interact. 16: 281-300.
71. Buening MK, Wislocki PG, Levin W, Yagi H, Thakker DR, Akagi H, Koreeda M, Jerina DM and Conney AH (1978) Tumorigenicity of the optical enantiomers of the diastereomeric benzo[a]pyrene 7,8-diol-9,10-epoxides in newborn mice: exceptional activity of (+)-7β,8α-dihydroxy-9α,10α- epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene. Proc. Natl. Acad. Sci. USA 75: 5358-5361.
72. Slaga TJ, Bracken WJ, Gleason G, Levin W, Yagi H, Jerina DM and Conney AH (1979) Marked differences in the skin tumor-initiating activities of the optical enantiomers of the diastereomeric benzo[a]pyrene 7,8-diol- 9,10- epoxides. Cancer Res. 39:67-71.
73. Cheng SC, Hilton BD, Roman JM and Dipple A (1989) DNA adducts from carcinogenic and noncarcinogenic enantiomers of benzo[a]pyrene dihydrodiol epoxide. Chem. Res. Toxicol. 2, 334-340.
74. Jerina DM, Chadha A, Cheh AM, Schurdak ME, Wood AW and Sayer JM (1991) Covalent bonding of bay-region diol epoxides to nucleic acids. Adv. Exp. Med. Biol. 283: 533-553.
75. Cosman M, de los Santos C, Fiala R, Hingerty BE, Singh SB, Ibanez V, Margulis LA, Live D, Geacintov NE, Broyde S and Patel DJ (1992) Solution conformation of the major adduct between the carcinogen (+)-anti-benzo- [a]pyrene diol epoxide and DNA. Proc. Natl. Acad. Sci. USA 89:1914-1918.
76. De los Santos C, Cosman M, Hingerty BE, Ibanez V, Margulis LA, Geacintov NE, Broyde S and Patel DJ (1992) Influence of benzo[a]pyrene diol epoxide chirality on solution conformations of DNA covalent adducts: the (-)-trans-anti-[BP]G·C adduct structure and comparison with the (+)-trans-anti-[BP]G•C enantiomer. Biochemistry 31: 9850-9863.
77. Cosman M, de los Santos C, Fiala R, Hingerty BE, Ibanez V, Luna E, Harvey RG, Geacintov NE, Broyde S and Patel DJ (1993) Solution conformation of the (+)-cis-anti-[BP]dG adduct in a DNA duplex: intercalation of the covalently attached benzo[a]pyrenyl ring into the helix and displacement of the modified deoxyguanosine. Biochemistry 32: 4145-4155.
78. Cosman M, Hingerty BE, Luneva N, Amin S, Geacintov NE, Broyde S and Patel DJ (1996) Solution conformation of the (-)-cis-anti-benzo[a]pyrenyl- dG adduct opposite dC in a DNA duplex: intercalation of the covalently attached BP ring into the helix with base displacement of the modified deoxyguanosine into the major groove. Biochemistry 35: 9850-9863.
79. Wu M, Yan SX, Patel DJ, Geacintov NE and Broyde S (2002) Relating repair susceptibility of carcinogen-damaged DNA with structural distortion and thermodynamic stability. Nucleic Acids Res. 30: 3422-3432.
80. Liu T, Xu J, Tsao H, Li B, Xu R, Yang C, Amin S, Moriya M and Geacintov NE (1995) Base sequence-dependent bends in site-specific benzo[a]pyrene diol epoxide-modified oligonucleotide duplexes. Chem. Res. Toxicol. 9:255-261.
81. Tsao H, Mao B, Zhuang P, Xu R, Amin S and Geacintov NE (1998) Sequence dependence and characteristics of bends induced by site-specific polynuclear aromatic carcinogen-deoxyguanosine lesions in oligonucleotides. Biochemistry 37: 4993-5000.
82. Geacintov NE, Cosman M, Hingerty BE, Amin S, Broyde S and Patel DJ (1996) NMR solution structures of stereoisomeric covalent polycyclic aromatic carcinogen-DNA adducts: principles, patterns, and diversity. Chem. Res. Toxicol. 10: 111-146.
83. Zou Y, Liu T, Geacintov NE and van Houten B (1995) Interaction of the UvrABC nuclease with a DNA duplex containing a single stereoisomer of dG-(+)- or dG-(-)-anti-BPDE. Biochemistry 34: 13582-13593.
84. Hecht SS, El-Bayoumy K, Rivenson A and Amin S (1994) Potent mammary carcinogenicity in female CD rats of a fjord region diol- epoxide of benzo[c]phenanthrene compared to a bay region diol-epoxide of benzo[a]pyrene. Cancer Res. 54: 21-24.
85. Levin W, Chang RL, Wood AW, Thakker DR, Yagi H, Jerina DM and Conney AH (1986) Tumorigenicity of optical isomers of the diastereomeric bay-region 3,4-diol-1,2-epoxides of benzo[c]phenanthrene in murine tumor models. Cancer Res. 46: 2257-2261.
86. Amin S, Krzeminski J, Rivenson A, Kurtzke C, Hecht SS and El-Bayoumy K (1994) Mammary carcinogenicity in female CD rats of fjord region diol epoxides of benzo[c]phenanthrene, benzo[g]chrysene, benzo[a]pyrene and dibenzo[a,l]pyrene. Carcinogenesis 16: 1971-1974.
87. Cavalieri EL, Higginbotham S, RamaKrishna NV, Devanesan PD, Todorovic R, Rogan EG and Salmasi S (1991) Comparative dose-tumorigenicity studies of dibenzo[a,l]pyrene versus 7,12-dimethylbenz[a]anthracene, benzo[a]pyrene and two dibenzo[a,l]pyrene dihydrodiols in mouse skin and rat mammary gland. Carcinogenesis 12: 1939-1944.
88. Higginbotham S, RamaKrishna NV, Johansson SL, Rogan EG and Cavalieri EL (1993) Tumor initiating activity and carcinogenicity of dibenzo[a,l]pyrene versus 7,12-dimethylbenz[a]anthracene and benzo[a]- pyrene at low doses in mouse skin. Carcinogenesis 14: 875-878.
89. Barbacid M (1987) Ras genes. Annu. Rev. Biochem. 56: 779-827.
90. Bos JL (1995) P21ras: an oncoprotein functioning in growth factor-induced signal transduction. Eur. J. Cancer 31 A: 1051-1054.
91. Lacal JC (1997) Regulation of proliferation and apoptosis by Ras and Rho GTPases through specific phospholipid-dependent signaling. FEBS Lett. 410: 73-77.
92. Bos JL (1989) Ras oncogenes in human cancer: a review. Cancer Res. 49: 4682-4689.
93. Gao HG, Chen JK, Stewart J, Song B, Rayappa C, Whong WZ and Ong T (1997) Distribution ofp53 and K-ras mutations in human lung cancer tissues. Carcinogenesis 18: 473-478.
94. Zhu D, Keohavong P, Finkelstein SD, Swalsky P, Bakker A, Weissfeld J, Srivastava S and Whiteside TL (1997) K-ras gene mutations in normal colorectal tissues from K-ras mutation-positive colorectal cancer patients. Cancer Res. 57: 2485-2492.
95. Marshall CJ, Vousden KH and Phillips DH (1984) Activation of c-Ha- ras-l proto-oncogene by in vitro modification with a chemical carcinogen, benzo[a]pyrene diol-epoxide. Nature 310: 586-589.
96. Vousden KH, Bos JL, Marshall CJ and Phillips DH (1986) Mutations activating human c-Ha-rasl protooncogene (HRAS1) induced by chemical carcinogens and depurination. Proc. Natl. Acad. Sci. USA 83: 1222-1226.
97. Balmain A and Pragnell IB (1983) Mouse skin carcinomas induced in vivo by chemical carcinogens have a transforming Harvey-ras oncogene. Nature 303: 72-74.
98. Dipple A, Pigott MA, Agarwal SK, Yagi H, Sayer JM and Jerina DM (1987) Optically active benzo[c]phenanthrene diol epoxides bind extensively to adenine in DNA. Nature 327: 535-536.
99. Quintanilla M, Brown K, Ramsden M and Balmain A (1986) Carcinogen- specific mutation and amplification of Ha-ras during mouse skin carcinogenesis. Nature 322: 78-80.
100. 1H NMR. Biochemistry 35: 6212-6224.
101. Geacintov NE, Broyde S, Buterin T, Naegeli H, Wu M, Yan S and Patel DJ (2002) Thermodynamics and structural factors in the removal of bulky DNA adducts by the nucleotide excision repair machinery. Biopolymers 65: 202-210.
102. Xu R, Mao B, Xu J, Li B, Birke S, Swenberg CE and Geacintov NE (1995) Stereochemistry-dependent bending in oligonucleotide duplexes induced by site-specific covalent benzo[a]pyrene diol epoxide-guanine lesions. Nucleic Acids Res. 23:2314-2319.
103. Cosman M, Fiala R, Hingerty BE, Laryea A, Lee H, Harvey RG, Amin S, Geacintov NE, Broyde S and Patel DJ (1993) Solution conformation of the (+)-trans-anti-[BPhJdA adduct opposite dT in a DNA duplex: intercalation of the covalently attached benzo[c]phenanthrene to the 5′-side of the adduct site without disruption of the modified base pair. Biochemistry 32: 12488-12497.
104. Cosman M, Laryea A, Fiala R, Hingerty BE, Amin S, Geacintov NE, Broyde S and Patel DJ (1995) Solution conformation of the (-)-trans-anti- benzo[c]phenanthrene-dA ([BPhJdA) adduct opposite dT in a DNA duplex: intercalation of the covalently attached benzo[c]phenanthrenyl ring to the 3′-side of the adduct site and comparison with the (+)-trans-anti- [BPh]dA opposite dT stereoisomer. Biochemistry 34: 1295-1307.
105. Krzeminski J, Ni JS, Zhuang P, Luneva N, Amin S and Geacintov NE (1999) Total synthesis, mass spectrometric sequencing, and stabilities of oligonucleotide duplexes with single trans-anti-BPDE-N6-dA lesions in the N-ras codon 61 and other sequence contexts. Polycycl. Aromat. Compds. 17:1-10.
106. 6-amino group to (-)-(7S,8R,9R,10S)-7,8-dihydroxy- 9,10-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene. Biochemistry 34:1364-1375.
107. Laryea A, Cosman M, Lin JM, Liu T, Agarwal R, Smirnov S, Amin S, Harvey RG, Dipple A and Geacintov NE (1995) Direct synthesis and characterization of site-specific adenosyl adducts derived from the binding of a 3,4-dihydroxy-1,2-epoxybenzo[c]phenanthrene stereoisomer toan 11-mer oligodeoxyribonucleotide. Chem. Res. Toxicol. 8: 444-454.
108. 6-adenine adducts: unusual thermal stabilization of modified DNA duplexes. Chem. Res. Toxicol. 15: 249-261.
109. Feng Z, Hu W, Chen JX, Pao A, Li H, Rom W, Hung MC and Tang MS (2002) Preferential DNA damage and poor repair determine ras gene mutational hotspot in human cancer. J. Natl. Cancer Inst. 94: 1527-1536.
110. Buschta-Hedayat N, Buterin T, Hess MT, Missura M and Naegeli H (1999) Recognition of nonhybridizing base pairs during nucleotide excision repair of DNA. Proc. Natl. Acad. Sci. USA 96: 6090-6095.
111. Hess MT, Schwitter U, Petretta M, Giese B and Naegeli H (1997) Bipartite substrate discrimination by human nucleotide excision repair enzymes. Proc. Natl. Acad. Sci. USA 94: 6664-6669.
112. RazinA (1998) CpG methylation, chromatin structure and gene silencing - a three-way connection. EMBO J. 17: 4905-4908.
113. Denissenko MF, Chen JX, Tang MS and Pfeifer GP (1997) Cytosine methylation determines hot spots of DNA damage in the human p53 gene. Proc. Natl. Acad. Sci. USA 94: 3893-3898.
114. Weisenberger DJ and Romano LJ (1999) Cytosine methylation in a CpG sequence leads to enhanced reactivity with benzo[a]pyrene diol epoxide that correlates with a conformational change. J. Biol. Chem. 274: 23948-23955.
115. Muheim R, Buterin T, Colgate KC, Kolbanovskiy A, Geacintov NE and Naegeli H (2003) Modulation of human nucleotide excision repair by 5-methylcytosines. Biochemistry 42: 3247-3254.
116. Huang X, Colgate KC, Kolbanovskiy A, Amin S and Geacintov NE (2002) Conformational changes of a benzo[a]pyrene diol epoxide-N(2)-dG adduct induced by a 5′-flanking 5-methyl-substituted cytosine in a (Me)CG doublestranded oligonucleotide sequence context. Chem. Res. Toxicol. 15:438-444.
117. Buterin T, Hess MT, Gunz D, Geacintov NE, Mullenders LH and Naegeli H (2002) Trapping of DNA nucleotide excision repair factors by nonrepairable carcinogen adducts. Cancer Res. 62: 4229-4235.
118. Cosman M, Fiala R, Hingerty BE, Amin S, Geacintov NE, Broyde S and Patel DJ (1994) Solution conformation of the (+)-trans-anti-[BP]dG adduct opposite a deletion site in a DNA duplex: intercalation of the covalently attached benzo[a]pyrene into the helix with base displacement of the modified deoxyguanosine into the major groove. Biochemistry 33: 11507-11517.
119. Cosman M, Fiala R, Hingerty BE, Amin S, Geacintov NE, Broyde S and Patel DJ (1994) Solution conformation of the (+)-cis-anti-[BP]dG adduct opposite a deletion site in a DNA duplex: intercalation of the covalently attached benzo[a]pyrene into the helix with base displacement of the modified deoxyguanosine into the minor groove. Biochemistry 33:11518-11527.
120. McLeod MC, Powell KL and Tran N (1995) Binding of the transcription factor Spl to non-target sites in DNA modified by benzo[a]pyrene diol epoxide. Carcinogenesis 16: 975-983.
121. 2-BPDE (7,8-dihydroxy-anti-9,10-epoxy-7,8,9,10- tetrahydrobenzo[a]pyrene). Biochemistry 41: 6100-6106.
122. 2-dG lesion catalyzed by the Y-family polymerase pol kappa. Biochemistry 42: 2456-2466.
123. 2-2 ′-deoxyguanosine adducts in Escherichia coli and simian kidney cells. Biochemistry 37: 10164-10172.
124. Yang JL, Maher VM and McCormick JJ (1987) Kinds of mutation formed when a shuttle vector containing adducts of (+)-7β,8α-dihydroxy-9α,10α- epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene replicates in human cells. Proc. Natl. Acad. Sci. USA 84: 3787-3791.
125. Zhu Y, Bye S, Stambrook PJ and Tischfield JA (1994) Single-base deletion induced by benzo [a]pyrene diol epoxide at the adenine phosphoribosyltrans- ferase locus in human fibrosarcoma cell lines. Mutat. Res. 321: 73-79.
126. Van Houten B, Illenye S, Yen Q and Farrell N (1993) Homodinuclear (Pt-Pt) and heterodinuclear (Ru-Pt) complexes as protein-DNA cross-linking agents: potential suicide DNA lesions. Biochemistry 32: 11794-11801.
127. Talaska G, Jaeger M, Reilman R, Collins T and Warshawsky D (1996) Chronic, topical exposure to benzo[a]pyrene induces relatively high steady- state levels of DNA adducts in target tissues and alters kinetics of adduct loss. Proc. Natl. Acad. Sci. USA 93: 7789-7793.
128. Naegeli H, Bardwell L and Friedberg EC (1992) The DNA helicase and adenosine triphosphatase activities of yeast Rad3 protein are inhibited by DNA damage. J. Biol. Chem. 267: 392-398.
129. Villani G and Le Gac NT (2000) Interactions of DNA helicases with damaged DNA: possible biological consequences. J. Biol. Chem. 275: 33185-33188.
130. Blow JJ (1993) Preventing re-replication of DNA in a single cell cycle: evidence for a replication licensing factor. J. Cell Biol. 122: 993-1002.